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Open Forum Infectious Diseases

MAJOR ARTICLE

The Increase in Hospitalizations for Urinary Tract


Infections and the Associated Costs in the United States,
1998–2011
Jacob E. Simmering,1 Fan Tang,2 Joseph E. Cavanaugh,3 Linnea A. Polgreen,4 and Philip M. Polgreen5
1
University of Iowa Health Venture’s Signal Center for Health Innovation, Iowa City; 2Genentech, San Francisco, California; 3Biostatistics, College of Public Health, University of Iowa, Iowa City;
4
Pharmacy Practice and Science, College of Pharmacy, University of Iowa, Iowa City; 5Internal Medicine, College of Medicine, and Epidemiology, College of Public Health, University of Iowa,
University of Iowa Health Venture’s Signal Center for Health Innovation, Iowa City

Background.  Outpatient therapies for urinary tract infections (UTIs) are becoming limited due to antimicrobial resistance. The
purpose of this paper is to report how the incidence of hospitalizations for UTIs have varied over time in both men and women
and across age groups. We also explore how the severity for UTI hospitalizations has changed and describe the seasonality of UTI
hospitalizations.
Methods.  Using the Nationwide Inpatient Sample, we compute a time-series of UTI incidence and subdivide the series by age
and sex. We fit a collection of time-series models to explore how the trend and seasonal intensity varies by age and sex. We modeled
changes in severity using regression with available confounders.
Results.  In 2011, there were approximately 400 000 hospitalizations for UTIs with an estimated cost of $2.8 billion. Incidence
increased by 52% between 1998 and 2011. The rate of increase was larger among both women and older patients. We found that the
seasonal intensity (summer peaks and winter troughs) increased over time among women while decreasing among men. For both
men and women, seasonality decreased with advancing age. Relative to controls and adjusted for demographics, we found that costs
among UTI patients grew more slowly, patients left the hospital earlier, and patients had lower odds of death.
Conclusions.  Incidence of UTI hospitalization is increasing and is seasonal, peaking in the summer. However, the severity of UTI
admissions seems to be decreasing, indicating that patients previously treated as outpatients may now be admitted to the hospital
due to increasing antimicrobial resistance.
Keywords.  healthcare costs; seasonality; time series; trends; urinary tract infections.

Urinary tract infections (UTIs) are among the most common antimicrobial resistance may have reduced the efficacy of tradi-
of all bacterial infections [1]. Half of all women experience tional outpatient treatments [7, 14, 15]. As the number of anti-
at least 1 UTI by the age of 35 [2], and approximately 20% of microbials resistant to outpatient therapies has risen, the number
women between the ages of 18 and 24 have a UTI annually [3, of hospitalizations for UTIs has also grown. Between 2000 and
4]. Urinary tract infections are a common reason for healthcare 2009, hospitalizations for UTIs increased dramatically [16].
visits. In the United States, UTIs result in an estimated 7 million However, it is not known how such an increase in hospitalizations
office visits, 1 million emergency department visits, and over has affected the estimates of healthcare costs attributable to UTIs.
100 000 hospitalizations with an associated annual cost of $1.6 Furthermore, it is not clear what subpopulations of patients are
billion [2, 5, 6]. driving this growth in incidence: the epidemiology of UTIs dif-
The majority of UTIs are treated on an outpatient basis [7]. fers between men and women and younger and older patients. In
However, resistance to first-line oral antimicrobials that are used addition, although the incidence of UTIs appears to be seasonal
to treat UTIs is increasing [4, 8–14], and this resistance com- [17–21], it is not clear how seasonality affects hospitalizations for
plicates outpatient treatment approaches: indeed, increasing UTIs, especially with respect to different populations of patients.
The purpose of this study is to describe the trends and sea-
Received 7 October 2016; editorial decision 29 December 2016; accepted 27 January 2017.
sonal patterns in the incidence of UTI hospitalizations by age
Correspondence: P. M. Polgreen, MD, MPH, Department of Internal Medicine, Carver College group and sex. In addition, we describe trends in length of stay,
of Medicine, University of Iowa, 200 Hawkins Dr., Iowa City, IA 52242 (philip-polgreen@uiowa.
inpatient mortality, and healthcare costs for hospitalizations
edu).
Open Forum Infectious Diseases® associated with UTIs.
© The Author 2017. Published by Oxford University Press on behalf of Infectious Diseases
Society of America. This is an Open Access article distributed under the terms of the Creative METHODS
Commons Attribution-NonCommercial-NoDerivs licence (http://creativecommons.org/licenses/
by-nc-nd/4.0/), which permits non-commercial reproduction and distribution of the work, in any Data Source and Case Definition
medium, provided the original work is not altered or transformed in any way, and that the
work is properly cited. For commercial re-use, please contact journals.permissions@oup.com.
Hospitalization data were obtained through the Agency for
DOI: 10.1093/ofid/ofw281 Healthcare Research and Quality Nationwide Inpatient Sample

Increase in UTI Incidence and Costs  •  OFID • 1


(NIS) for the years 1998 to 2011. The NIS contains a 20% strat- Specifically, changes over time would have affected cases and
ified sample of all hospitals in the United States. Each record controls differently. In contrast, length of stay, mortality, and
represents a single hospitalization that includes diagnoses, pro- costs (after adjustment for inflation) exist on a standard scale
cedures, demographic, and other information about the patient. that does not vary over time, and any changes would affect cases
Cases were defined as any inpatient stay with a primary diagno- and controls in the same way. We used data from 100% of UTI
sis International Classification of Diseases, Ninth Revision (ICD- cases, but we only retained data on a randomly selected 10%
9) code of 599.0 (“Urinary tract infection, site not specified”). subsample of controls to reduce the computational demands of
We excluded records for patients under 18 years of age or that model fitting. Because the 10% subsample is approximately 7
did not include values for month, year, age, and patient sex. times larger than the number of UTI cases, there is little effect
Case counts were normalized to incidence rates with the mid- of this sampling on our estimation. We excluded any of the
year population estimates from the Census Bureau by each spe- cases or controls that had a labor and delivery diagnosis code
cific combination of sex and age category. Age categories were on their record (ICD 9 codes: 650, 651, 652, 669.5, 669.6, or
defined as 18–29, 30–39, 40–49, 50–59, 60–69, 70–79, and over 669.7), to reduce confounding by these stays in young women.
90 years old. To facilitate comparisons among the groups, the We only considered length of stay in cases in which the patient
incidence in some analyses was converted to age-sex-specific was discharged alive to avoid truncation due to death. Total
Z-scores (Z = (observation – mean)/standard deviation). charges were converted to total cost using the Healthcare Cost
and Utilization Project (HCUP)-provided cost-to-charge ratios.
Statistical Analysis
When possible, we used the all-payer hospital-specific ratio.
Trend Estimation
If the hospital-specific ratio was not reported, we used the
An autoregressive moving average (ARMA) model with a sea-
group-average all-payer ratio. These ratios are only available for
sonal autoregressive component of order 1 was used to charac-
years 2001–2011. After conversion to total costs, we applied the
terize the data. A linear trend was incorporated as an exogenous
Consumer Price Index for Medical Care [22] to convert all dol-
regressor in the ARIMA model to account for the increase in
lar amounts to constant December 2011 dollars.
UTI cases. Based on the ARMA framework, we can estimate the
We estimate changes in length of stay, mortality, and costs
trend effect while simultaneously controlling for the temporal
using traditional linear regression or logistic regression models,
correlation inherent in time-series data. A separate model was
as appropriate. We regressed each outcome on the patient age (an
fit for each combination of sex and age (eg, males 18–29, males
indicator for each decade), sex, number of procedures performed
30–39…), where the standardized incidence was regressed on
during the stay, month of year, an indicator for UTI as primary
a year index (year  +  (month  –  1)/12) and the month of the
diagnosis, the year, and the interaction between year and the UTI
patient’s discharge. The year variable accounts for long-term
indicator. The primary coefficient of interest is on this interaction
changes over time, and the month variable captures seasonal-
term: it reflects the slope difference between the linear trend of
ity—annual periodicities as reflected in changes by month.
non-UTI and UTI patients. For the regression parameter esti-
mates, we used heteroskedastic-consistent standard errors.
Seasonal Estimation
To further examine UTI seasonality, we detrended the series:
Sensitivity Analysis
a linear trend was fit to each of the subseries described above,
Because it is possible that some of the change in incidence of
and the residuals were obtained. The resulting residuals are a
UTIs could have been associated with changes in coding or
series that has a constant mean (no trend) but retains the sea-
diagnostic approaches, as a sensitivity analysis, we considered
sonal fluctuations. For each series, we computed the yearly
trends in incidence for pyelonephritis (ICD-9-CM codes of 590.
maximum, minimum, and range observed in these residuals.
xx) relative to trends for UTIs. Pyelonephritis is a more severe
We also computed the mean patient age within each of the age
diagnosis, and regardless of antimicrobial resistance patters of
groups used to create the series. We stratified the resulting data
the causative agent, it is more likely to lead to hospitalization
by sex. We estimated the effects of increasing age and increas-
than the diagnosis of an UTI. Thus, we computed monthly
ing year by regressing the observed maximum, minimum, and
incidence series for pyelonephritis and UTIs and estimated the
range on the mean age and the year with separate models for
trend using the ARMA framework explained above.
men and women.

RESULTS
Severity Estimation
Next, we consider length of stay, inpatient mortality, and For the years 1998 to 2011, there were 108 672 713 hospital
costs for UTI and non-UTI admissions. We used these meas- admissions in the NIS. Of these, 960 516 were for UTIs in
ures of severity as opposed to an index such as the Charlson adults. The data required to construct the time series (age, sex,
or Elixhauser comorbidity coding systems due to concerns admission year, and month) were present on 860 870 of these
about the lack of time invariance of the comorbidity systems. records. Somewhat smaller samples were used for the severity

2 • OFID • Simmering et al
models due to the additional variables required (eg, length of tract infections peak in the summer months and the nadir
stay, mortality) (sample sizes are reported with the regressions). occurs during the winter. The incidence of admissions for UTIs
exhibits a stronger seasonal effect for women than for men.
Summary Statistics
Seasonality is most pronounced among younger patients, and it
Weighted summary statistics of the sample are included in
diminishes with advancing age. Among women, for each year of
Table 1. Between 1998 and 2011, the number of UTI admissions
age there was a decrease of 2.6% of a standard deviation in the
increased from 264 404 (12.9 per 10 000 people) to 436 635 (18.4
range of the seasonal intensity. Among men, for each year of age
per 10 000 people). The majority of the increase in admissions
there was a decrease of 1.0% of a standard deviation. During our
occurred among women (67.7% in 1998, 71.4% in 2011). The
study period, the seasonal intensity changed. Among women,
mean age of UTI patients with a primary diagnosis of a UTI
the seasonality increased: the incidence of UTIs for women at
increased from 73.2 to 74.7 years. Mean length of stay decreased
the beginning of our sample was less seasonal than at the end. In
from 5.29 to 4.24 days. For UTI hospitalizations, average real total
contrast, among men, the seasonality diminished. Specifically,
costs increased from $3368 to $6425 between 2001 and 2011. The
with each passing year between 1998 and 2011, the average
20th and 80th percentiles of costs in 2011 were $3113 and $8409,
seasonal intensity increased by 3.0% of a standard deviation in
respectively. The median real total costs increased from $2365 to
women and decreased by 4.5% of a standard deviation in men.
$5019. A plot of total charges over time is shown in Figure 1.
Trend Estimation Severity Estimation

Incidence of hospital admissions for UTIs increased in both Length of stay decreased in both UTI and non-UTI hospi-
men and women of all ages (Table  2). The number of cases talizations. However, in a model adjusting for age (grouped by
increased by 76% over the study period, and incidence (pop- decade), sex, year, month of year, number of procedures, and a
ulation adjusted) increased by 52%. Incidence rates acceler- primary diagnosis of an UTI, we found that the length of stay
ated with advancing age: the growth rate for 18- to 29-year-old decreased faster for patients with a primary diagnosis of an UTI
women was 7.9% of a standard deviation per year, whereas the (Table 4). Specifically, a non-UTI patient stayed an average of
growth rate for 80- to 89-year-old women was 23.1%. Although 13.1 (P < .0001) fewer hours in 2011 compared with 1998; how-
UTI incidence was rising for all sex and age groups, the aver- ever, UTI patients stayed an average of 27.7 (P < .0001) fewer
age rate of increase for women was approximately twice the rate hours—a difference of 14.6 hours (P < .0001).
of increase in men. For example, the rate of increase for 50- to Inpatient mortality decreased substantially between 1998
59-year-old men was 9.8% of a standard deviation per year and and 2011 (Table 4). In general, the odds of inpatient death for
for 50- to 59-year-old women, 19.2%. non-UTI patients decreased by 3% per year. Urinary tract infec-
tion patients, on the other hand, observed an extra 5% (odds
Seasonal Estimation
ratio, 0.95; 95% condidence interval [CI], .94–.95) reduction in
The incidence of UTI hospitalizations is highly seasonal
the odds of death per year for a total of 8% decrease in the odds
and our seasonality findings are reported in Table  3. Urinary
of death per year for UTI patients. Thus, for non-UTI patients,
their odds of death were 35% lower in 2011 than in 1998. In
contrast, for UTI patients, their odds of death were 68% lower
Table  1.  Weighted Baseline Characteristics of UTI Admissions in NIS,
1998–2011 in 2011 than in 1998.
Costs increased for all patients between 1998 and 2011
Variable Name Count/Mean Percent/SD (Table 4). Among non-UTI patients, there was an average
Age 74.03 16.62 yearly increase of $577 (P < .0001). In contrast, UTI patients
Female 2 935 344 69.05% had yearly increases of $317, a difference of $259 (P < .0001)
Race
per year.
 White 2 454 310 74.90%
In 2011, more than 436 437 patients were admitted with a
 Black 424 712 12.96%
 Hispanic 245 948 7.51% primary diagnosis of UTI. These hospitalizations resulted in
 Asian 62 150 1.90% charges of $9.7 billion and a real total cost of $2.8 billion for
  Native American 16 535 0.50% these UTI admissions. The mean real cost per case has increased
 Other 73 252 2.24% by 90.8% and non-UTI mean real cost has increased by more
Length-of-Stay 4.77 5.11
than 123.0% between 2001 and 2011.
Died 74 480 1.75%
Total Charges Sensitivity Analysis
 Mean 13 671 18 940
The incidence rate for pyelonephritis was 4.7 cases per 10 000
 Median 8682
Number of Procedures 0.50 1.09
people in 1998, and it increased by 2.7% to 4.8 cases per 10 000
people in 2011. Monthly incidence is shown in Figure 2. Our
Abbreviations: NIS, nationwide inpatient sample; SD, standard deviation; UTI, urinary tract
infection. regression analysis showed the monthly incidence increased by

Increase in UTI Incidence and Costs  •  OFID • 3


Number of UTI Cases / Month
25000

20000

15000

10000

5000 Gender
Men
Total Cost (Millons of 2011 Dollars) / Month
160 Women

120

80

40

2000 2004 2008 2012

Figure 1.  Urinary tract infection (UTI) incidence and total cost of hospitalizations by sex, 1998–2011. Incidence is the number of cases per 10 000 people in the community
by sex, and real total costs are converted to costs using the Healthcare Cost and Utilization Project cost-to-charge ratio and are normalized to constant December 2011 dollars.
Solid lines denote the male series, whereas dotted lines represent the female series.

0.002 more cases per 10 000 people every year (95% CI, −.001 to primary diagnosis of UTI cost $3368 in 2001 and $6424 in
.005). This compares to the 42.6% increase in incidence for UTIs 2011 (constant December 2011 dollars). The 436 437 cases
between 1998 and 2011, and our regression analysis showed an hospitalized in 2011 resulted in a total cost of $2.8 billion in
increase in the monthly incidence of UTIs of 0.04 more cases healthcare cost.
per 10 000 people every year (95% CI, .028–.044). These increases in incidence were only observed among UTIs.
The incidence of pyelonephritis remained relatively flat between
DISCUSSION 1998 and 2011. In addition, the rate of growth over time in pye-
We found a dramatic increase in the incidence of hospitaliza- lonephritis incidence was not statistically significantly different
tions attributable to UTIs from 1998 to 2011: cases increased from zero (0.002 [95% CI, −.001 to .005] higher monthly inci-
by 76% and incidence increased by 52%. The greatest increase dence per 10 000 people), whereas UTI incidence was increas-
in the number of hospitalizations for UTIs occurred among ing (0.04 [95% CI, .028–.044] higher monthly incidence per
women, which is not surprising. Although UTIs are most 10 000 people every year). Assuming that patients with pyelo-
common in younger women, our results demonstrated that nephritis are more likely to be hospitalized than patients with
most of the increase in UTI hospitalizations occurred among UTIs because of their more severe symptoms, regardless of the
older women (eg, patients older than 70). Urinary tract infec- resistance of the causative pathogen, we believe that these find-
tion hospitalizations also increased for men, especially among ings are consistent with our theory that antimicrobial resistance
older men. These dramatic changes in incidence of UTI hos- was driving some of the increase in incidence in hospitaliza-
pitalizations that we report highlight the need to re-estimate tions for patients with a primary diagnosis of an UTI between
costs attributable to UTIs. An average hospitalization with a 1998 and 2011. The relatively faster growth in incidence for

Table  2.  Yearly Trend Estimates From ARMA Models Expressed as the Percentage of a Standard Deviation Increase per Year in UTI Hospitalization
Incidence

Age Group Trend in Men Trend in Men, Standard Error Trend in Women Trend in Women, Standard Error

18–29 6.8% 2.1% 7.9% 3.0%


30–39 2.2% 2.5% 14.6% 2.4%
40–49 6.9% 2.4% 17.1% 2.2%
50–59 9.8% 2.9% 19.2% 1.9%
60–69 6.8% 3.4% 19.7% 2.0%
70–79 12.3% 3.2% 22.4% 1.4%
80–89 14.4% 2.6% 23.1% 1.6%
90+ 12.3% 2.4% 21.4% 1.7%

Abbreviations: ARMA, autoregressive moving average; UTI, urinary tract infection.

4 • OFID • Simmering et al
Table 3.  Effects of Age and Admission Year on Seasonal Intensity of UTI Hospitalization Incidence in Men and Women

Range Minimum Maximum

Effect in Men
Variable Name Effect in Men (SD) Effect in Women (SD) (SD) Effect in Women (SD) Effect in Men (SD) Effect in Women (SD)
† ‡
Patient age −0.010 (0.003)* −0.026 (0.002)* 0.004 (0.002) 0.012 (0.002)* −0.007 (0.003) −0.014 (0.001)*
Admission year −0.045 (0.015)‡ 0.030 (0.010)‡ 0.024 (0.011)§ −0.015 (0.009)† −0.021 (0.014) 0.015 (0.008)†
R2 0.177 0.689 0.072 0.388 0.080 0.471

Abbreviations: SD, standard deviation; UTI, urinary tract infection.


*P < .001.

P < .1.

P < .01.
§
P < .05.  

UTIs compared with pyelonephritis is also suggestive of anti- uropathogens resistant to first-line antimicrobial treatments.
microbial resistance as a driver of the dramatic increase in the Converting only a small fraction of patients from inpatient to
incidence of hospitalizations for UTIs rather than changes in outpatient treatment would lead to a large number of patients
coding or changes in diagnostic practices. being able to avoid a hospitalization, given that the median
Our study period coincided with reports of increases in anti- UTI hospitalization costs $4500, whereas the cost for outpa-
microbial resistance for agents commonly used to treat UTIs tient treatment is significantly less expensive. Shifting patients
[8, 12–14, 16]. Thus, the increase in incidence of admissions we from inpatient admissions to outpatient treatment could lead
report is most likely associated with the inability to treat UTIs to considerable cost savings. In lieu of new oral antibiotics,
in outpatient settings due to increased resistance. If some of innovative approaches to provide IV antibiotic therapy at
the increase in incidence in admissions was driven by patients home or in outpatient settings provides alternative cost-sav-
who would have otherwise been treated as an outpatient, we ing approaches; however, payer barriers remain an important
would expect to see a trend toward the admission of less-severe limitation [23].
patients, ie, patients who were only admitted for treatment with For both men and women, the annual rate of growth in inci-
intravenous (IV) antimicrobials. Indeed, in terms of severity, we dence of admissions for UTIs increased with age. For the oldest
found that the patients admitted at the beginning of our study men in our study population, the UTI rate increased at twice
period differed from those at the end. Specifically, compared the rate of the youngest men. For the oldest women, the UTI
with controls, costs grew at a 45% slower annual rate for UTI rate increased at almost 3 times the rate of the youngest women.
patients, length of stay fell 110% faster for UTI patients, and the Thus, older patients seem to be disproportionally contributing
odds of death for UTI patients fell at a 105% faster rate. We posit to the increase in hospitalizations. If the increase in incidence of
that these less severe patients represent patients who would admissions for UTI is being driven at least in part by antimicro-
have previously been treated as outpatients with oral antimi- bial resistance, it follows that older patients are more likely to be
crobial agents. affected, given that older patients are more likely to have contact
The dramatic increase in hospitalizations for UTIs sug- with the healthcare system and are more likely to be exposed
gests the need for oral antibiotics or IV treatments convenient to multidrug-resistant organisms. However, given that we did
to administer in outpatient settings that are effective against observe an increase in admissions among women of all ages, as

Table 4.  Adjusted Changes in Severity Measures for Control and UTI Patients per Year Between 1998 and 2011a 

Variable Name Change in Controls Change in UTI Patients Difference (SD) Difference as Percentage

Cost (dollars) 576.71 317.24 −259.47 (2.64)* −45%


(n = 6 374 024)
Length-of-stay (hours) −0.936 −1.968 −1.032 (0.024)* +10%
(n = 8 517 901)
Inpatient death 0.97 0.92 0.95 (95% CI, .94–.95)* −5%
(n = 8 734 469)

Abbreviations: CI, confidence interval; SD, standard deviation; UTI, urinary tract infections. 
a
Note that the “change in UTI patients” column is simply the combination of the “change in controls” and “difference” columns (addition for linear models, multiplication for the odds ratios).
*P < .0001.

Increase in UTI Incidence and Costs  •  OFID • 5


Monthly Incidence per 10,000 people
1.2

Diagnosis
Pyelonephritis
UTI
0.8

0.4

2000 2005 2010


Year

Figure 2.  Urinary tract infection (UTI) and pyelonephritis incidence, 1998–2011. Incidence is the number of cases per 10 000 people by month.

multidrug resistance spreads, we may see a further increase in and thus we could not directly incorporate information regard-
hospitalizations among younger women. ing therapies or antimicrobial drug resistance. In addition, we
We observed a strong pattern of seasonality for UTI hospi- were unable to review charts to validate the assignment of diag-
talizations among both men and women of all ages: UTI inci- nostic codes. Second, in our database, we only observed events
dence increases in the summer and decreases in the winter. from inpatient admissions and did not observe outpatient UTI
Reports of seasonality have mostly been restricted to single incidence, and the majority of patients were treated on an out-
centers [17, 18]. However, Internet search terms for UTI are patient basis; thus, our study was focused only on more severe
seasonal in countries around the world [24]. Also of note, we or difficult-to-treat cases. Third, our data source did not include
found that the changes in the degree of seasonality vary by sex. a unique identifier to link visits over time. Thus, we could not
During our study period, the seasonality of hospitalizations for identify patients first treated as outpatients and later admitted
UTIs decreased with age for men and women: younger men to the hospital for UTIs, nor could we investigate the incidence
and women experience more seasonality than older men and among patients with a history of recurrent UTI admissions.
women. However, over time, the seasonal range increased for Fourth, the decreases in length of stay that we observed may
women and decreased for men: specifically, for each year of have beeen due to improvements in treatment that occurred
our study period, UTIs became more seasonal for women and during the study period.
less seasonal for men. Although the differences in risk factors Despite our limitations, we show that the incidence of admis-
for and epidemiology of UTIs between men and women are sions for UTIs have increased dramatically, especially among
well known [7, 25, 26], our findings suggest additional differ- older patients and women. We also show that patients admit-
ences, highlighting the need to think about different preventive ted for UTIs, on average, appear to be relatively less severe than
approaches for men and women. Prevention approaches also in prior years. Our results are consistent with what we would
may need to differ by age group. expect to find from increasing antimicrobial resistance, ie,
Although it is unclear why the incidence for UTIs is seasonal, increasing rates of hospitalization, increasing total cost, and
weather has been associated with the seasonality of several dis- decreasing average severity among patients admitted with a pri-
eases [20, 27–30]. It is noteworthy to mention that blood stream mary diagnosis of an UTI. Although, our results provide evi-
infections with Gram-negative organisms are seasonal and are dence that antimicrobial resistance may be driving healthcare
associated in some cases with higher temperatures [19, 21, 31, costs, future studies with antimicrobial data at the patient level
32], and most of these blood stream infections could have orig- are needed to confirm our findings. 
inated as UTIs. Further exploration of the seasonality of UTIs
by, for example, adding weather data, may lead to better under- CONCLUSIONS
standing of the cause of this seasonality of UTIs. Finally, our results demonstrate the need for (1) new oral or
Our study has limitations. First, we exclusively used adminis- single-dose antimicrobial agents that can administered in out-
trative data and did not have medication or microbiology data, patient settings, (2) focused stewardship efforts on patients with

6 • OFID • Simmering et al
UTIs, and (3) innovative approaches to treat UTI patients with Infection Collaborative Alliance (NAUTICA). Int J Antimicrob Agents 2006;
27:468–75.
resistant pathogens on an outpatient basis. Reducing hospitali- 13. Olson RP, Harrell LJ, Kaye KS. Antibiotic resistance in urinary isolates of
zations due to resistant organisms may represent “low-hanging Escherichia coli from college women with urinary tract infections. Antimicrob
Agents Chemother 2009; 53:1285–6.
fruit” in an effort to control hospitalization costs and prevent 14. Sanchez GV, Master RN, Karlowsky JA, Bordon JM. In vitro antimicrobial resist-
hospitalizations. ance of urinary Escherichia coli isolates among U.S. outpatients from 2000 to 2010.
Antimicrob Agents Chemother 2012; 56:2181–3.
15. Raz R, Chazan B, Kennes Y, et  al. Empiric use of trimethoprim-sulfamethoxa-
Acknowledgments
zole (TMP-SMX) in the treatment of women with uncomplicated urinary tract
Financial support.  This work was funded by the National Heart, Lung infections, in a geographical area with a high prevalence of TMP-SMX-resistant
and Blood Institute at the National Institutes of Health (Grant number uropathogens. Clin Infect Dis 2002; 34:1165–9.
K25HL 122305; to L. A. P.), the University of Iowa Health Ventures’ Signal 16. Zilberberg MD, Shorr AF. Secular trends in gram-negative resistance among
Center (to P.  M. P.), and a dissertation fellowship from the University of urinary tract infection hospitalizations in the United States, 2000–2009. Infect
Iowa College of Pharmacy (to J. E. S.). Control Hosp Epidemiol 2013; 34: 940–6.
Potential conflicts of interest.  All authors: No reported conflicts. 17. Anderson JE. Seasonality of symptomatic bacterial urinary infections in women.
J Epidemiol Community Health 1983; 37:286–90.
The authors have submitted the ICMJE Form for Disclosure of Potential
18. Stamm WE, McKevitt M, Roberts PL, White NJ. Natural history of recurrent uri-
Conflicts of Interest. Conflicts that the editors consider relevant to the con-
nary tract infections in women. Rev Infect Dis 1991; 13:77–84.
tent of the manuscript have been disclosed. 19. Perencevich EN, McGregor JC, Shardell M, et al. Summer Peaks in the incidences
of Gram-negative bacterial infection among hospitalized patients. Infect Control
Hosp Epidemiol 2008; 29:1124–31.
References 20. Falagas ME, Peppas G, Matthaiou DK, et al. Effect of meteorological variables on
1. Nicolle LE. Epidemiology of urinary tract infections. Clin Microbiol Newsletter the incidence of lower urinary tract infections. Eur J Clin Microbiol Infect Dis
2002; 24:135–40. 2009; 28:709–12.
2. Foxman B, Barlow R, D’Arcy H, et al. Urinary tract infection: self-reported inci- 21. Al-Hasan MN, Lahr BD, Eckel-Passow JE, Baddour LM. Seasonal variation in
dence and associated costs. Ann Epidemiol 2000; 10:509–15. Escherichia coli bloodstream infection: a population-based study. Clin Microbiol
3. Hooton TM, Scholes D, Hughes JP, et  al. A prospective study of risk factors Infect 2009; 15:947–50.
for symptomatic urinary tract infection in young women. N Engl J Med 1996; 22. US Bureau of Labor Statistics. Consumer Price Index for All Urban Consumers:
335:468–74. Medical Care (CPIMEDSL). Available at: https://fred.stlouisfed.org/series/
4. Brown PD, Freeman A, Foxman B. Prevalence and predictors of trimethop- CPIMEDSL. Accessed 18 July 2016.
rim-sulfamethoxazole resistance among uropathogenic Escherichia coli isolates in 23. Bhavan KP, Brown LS, Haley RW. Self-administered outpatient antimicrobial
Michigan. Clin Infect Dis 2002; 34:1061–6. infusion by uninsured patients discharged from a safety-net hospital: a propensi-
5. Stamm WE, Hooton TM. Management of urinary tract infections in adults. N ty-score-balanced retrospective cohort study. PLoS Med 2015; 12:e1001922.
Engl J Med 1993; 329:1328–34. 24. Rossignol L, Pelat C, Lambert B, et al. A method to assess seasonality of urinary
6. Foxman B. Epidemiology of urinary tract infections: incidence, morbidity, and tract infections based on medication sales and google trends. PLoS One 2013;
economic costs. Am J Med 2002; 113:5S–13S. 8:e76020.
7. Gupta K, Hooton TM, Naber KG, et al. International clinical practice guidelines for 25. Hooton TM. Uncomplicated urinary tract infection. N Engl J Med 2012;
the treatment of acute uncomplicated cystitis and pyelonephritis in women: a 2010 366:1028–37.
update by the Infectious Diseases Society of America and the European Society for 26. Scholes D, Hooton TM, Roberts PL, et al. Risk factors associated with acute pye-
Microbiology and Infectious Diseases. Clin Infect Dis 2011; 52:e103–20. lonephritis in healthy women. Ann Intern Med 2005; 142:20–7.
8. Karlowsky JA, Jones ME, Thornsberry C, et al. Prevalence of antimicrobial resist- 27. Falagas ME, Theocharis G, Spanos A, et al. Effect of meteorological variables on
ance among urinary tract pathogens isolated from female outpatients across the the incidence of respiratory tract infections. Respir Med 2008; 102:733–7.
US in 1999. Int J Antimicrob Agents 2001; 18:121–7. 28. Fisman D. Seasonality of viral infections: mechanisms and unknowns. Clin
9. Kahlmeter G. Prevalence and antimicrobial susceptibility of pathogens in uncom- Microbiol Infect 2012; 18:946–54.
plicated cystitis in Europe. The ECO.SENS study. Int J Antimicrob Agents 2003; 29. Fisman DN. Seasonality of infectious diseases. Annu Rev Public Health 2007;
22:49–52. 28:127–43.
10. Kahlmeter G; ECO.SENS. An international survey of the antimicrobial suscepti- 30. Fisman DN, Lim S, Wellenius GA, et al. It’s not the heat, it’s the humidity: wet
bility of pathogens from uncomplicated urinary tract infections: the ECO.SENS weather increases legionellosis risk in the greater Philadelphia metropolitan area.
Project. J Antimicrob Chemother 2003; 51:69–76. J Infect Dis 2005; 192:2066–73.
11. Metlay JP, Strom BL, Asch DA. Prior antimicrobial drug exposure: a risk factor for 31. Freeman JT, Anderson DJ, Sexton DJ. Seasonal peaks in Escherichia coli infections:
trimethoprim-sulfamethoxazole-resistant urinary tract infections. J Antimicrob possible explanations and implications. Clin Microbiol Infect 2009; 15:951–3.
Chemother 2003; 51:963–70. 32. Schwab F, Gastmeier P, Meyer E. The warmer the weather, the more Gram-
12. Zhanel GG, Hisanaga TL, Laing NM, et al. Antibiotic resistance in Escherichia coli negative bacteria—impact of temperature on clinical isolates in intensive care
outpatient urinary isolates: final results from the North American Urinary Tract units. PLoS One 2014; 9:e9115.

Increase in UTI Incidence and Costs  •  OFID • 7

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